Antibacterial Properties of Silver Nanoparticles Embedded on Polyelectrolyte Hydrogels Based on Α-Amino Acid Residues

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Antibacterial Properties of Silver Nanoparticles Embedded on Polyelectrolyte Hydrogels Based on Α-Amino Acid Residues gels Article Antibacterial Properties of Silver Nanoparticles Embedded on Polyelectrolyte Hydrogels Based on α-Amino Acid Residues Mario Casolaro 1,*, Ilaria Casolaro 2, Jun Akimoto 3, Motoki Ueda 3 ID , Masashi Ueki 3 and Yoshihiro Ito 3 ID 1 Dipartimento di Biotecnologie, Chimica e Farmacia (Dipartimento di Eccellenza 2018–2022), Università degli Studi di Siena, via A. Moro, 2-53100 Siena, Italy 2 ASST Valtellina e Alto Lario, Dipartimento di Salute Mentale, via Stelvio, 25-23100 Sondrio, Italy; [email protected] 3 Nano Medical Engineering Laboratory, Riken, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan; [email protected] (J.A.); [email protected] (M.U.); [email protected] (M.U.); [email protected] (Y.I.) * Correspondence: [email protected]; Tel.: +39-0577-234388 Received: 5 April 2018; Accepted: 2 May 2018; Published: 4 May 2018 Abstract: Polyelectrolyte hydrogels bearing L-phenylalanine (PHE), L-valine (AVA), and L-histidine (Hist) residues were used as scaffolds for the formation of silver nanoparticles by reduction of Ag+ ions with NaBH4. The interaction with the metal ion allowed a prompt collapse of the swollen hydrogel, due to the neutralization reaction of basic groups present on the polymer. The imidazole nitrogen of the hydrogel with Hist demonstrated greater complexing capacity with the Ag+ ion compared to the hydrogels with carboxyl groups. The subsequent reduction to metallic silver allowed for the restoration of the hydrogel’s degree of swelling to the starting value. Transmission electron microscopy (TEM) and spectroscopic analyses showed, respectively, a uniform distribution of the 15 nm spherical silver nanoparticles embedded on the hydrogel and peak optical properties around a wavelength of 400 nm due to the surface plasmonic effect. Unlike native hydrogels, the composite hydrogels containing silver nanoparticles showed good antibacterial activity as gram+/gram− bactericides, and higher antifungal activity against S. cerevisiae. Keywords: polyelectrolyte hydrogels; silver nanoparticles; equilibrium degree of swelling; TEM; antimicrobial activities 1. Introduction Today it is widely accepted that polymeric materials are extremely useful in various fields of science and technology. In particular, cross-linked polymers (hydrogels) play a fundamental role for various biomedical purposes due to their compatibility with soft tissues [1–3]. Since hydrogels have structural and compositional similarities with respect to extracellular matrices and their broad structure for cell proliferation and survival, they have for a long time attracted considerable attention in biomedicine. Hydrogels are materials capable of retaining a large amount of water inside their porous structure and are therefore subject to deformation due to external triggers [3]; among these we can include direct stimuli (pH, temperature, ionic strength) or remote stimuli (alternating magnetic field, light). A series of polyelectrolyte hydrogels bearing α-amino acid residues (L-valine, L-phenylalanine, L-histidine), which better approximate the properties of biological tissues consisting of filamentous polyelectrolyte proteins, have been studied for many years (Scheme1)[3–5]. Gels 2018, 4, 42; doi:10.3390/gels4020042 www.mdpi.com/journal/gels Gels 2018, 4, 42 2 of 15 Scheme 1. Structure of poly(N-acryloyl-L-phenylalanine), poly(N-acryloyl-L-valine), and poly(N- acryloyl-L-histidine). The presence of ionic/ionizable functional groups (carboxyl, amine) allows these hydrogels to complex metal ions and/or drug molecules, also based on metals, for their better use in controlled release in different and relevant therapies [6]. The hydrogels behave as containers of drugs that, in addition to preserving the drug itself from possible degradation, control its release kinetics in the surrounding environment by virtue of the polymer–drug ionic interaction force. The studies previously reported for the release of cisplatin [7,8] and other metal-based drugs [9,10], as well as the release of anticancer drugs (doxorubicin) [11], treatment of glaucoma (pilocarpine) [12], and antidepressants (trazodone, citalopram, paroxetine, duloxetine, vortioxetine) [13–15], confirm that the main polymer–drug interaction is ionic in nature; the strength of this interaction influences the whole release process, with the free drug molecule, in equilibrium with the adduct, which diffuses through the hydrogel network to be finally used for therapeutic purposes. The strength of this interaction is attributed to the basicity constants (pKa) values of the ionic groups involved in the process: carboxyl group of the hydrogel and amine group of the drug. In general, and with the same hydrogel in the swollen state, a greater pKa of the cationic drug produces a more rapid and complete collapsing phenomenon. In this paper we propose to report the behavior of the hydrogels mentioned above against the silver ion in solution and its subsequent reduction to metallic silver in the form of nanoparticles. Silver nanoparticles, used in a variety of technologies, are incorporated into numerous consumer products to benefit from their unique conductive, optical, and primarily antibacterial properties [16]. Silver nanoparticles have become increasingly popular for antimicrobial coatings, especially in biomedical devices, as the continuous release of a low level of silver ions provides protection against bacteria [17,18]. As is well known, biofouling, i.e., the accumulation of bacteria on material surfaces, is a worldwide problem that many researchers have taken into account. Various antibacterial reagents such as chitosan, quaternary ammonium salts, and metal ions are employed to enhance the antibacterial properties of membranes [19,20]. Some years ago, we developed a new type of copolymer composed of L-histidine (ampholyte) and n-butyl methacrylate (hydrophobic moiety) for the preparation of nonbiofouling surfaces [21]. More recently, Wang et al. proposed a straightforward mussel-inspired approach to construct chitosan–polyurethane coatings and load Ag nanoparticles to endow polyethersulfone membrane with dual antibacterial and antifouling properties [22]. Moreover, a substrate-independent Ag-nanoparticle-loaded temperature-sensitive hydrogel coating was synthesized and covalently attached onto a model substrate. The coating showed good hemo- and cytocompatibility, and the effect of temperature revealed cell detachment properties on various medical devices [23]. To date, a universal approach for fabricating low-cost antifouling surfaces is based on tannic acid and a novel reactive zwitterionic polymer [24]. Gels 2018, 4, 42 3 of 15 The use of hydrogels, synthetic and natural, can contribute to the development of theranostic agents for more specific clinical therapies [25]. The development of microcontainers is attractive for applications in biomedicine and cell biology. Such an example of biocompatible hollow microcapsules, alginate matrix, and silver nanoparticles, where the silver alginate hydrogel microcapsules serve as microcontainers with a functional substance payload, has recently been reported by Lengert et al. [26]. As well as other synthetic hydrogels, based on acrylates, they were studied as composites and multifunctional orthopedic hydrogels such as osseoconductive and non-antibiotic based antibacterial [27]. Also, other nanocomposites based on acrylic copolymers and containing ionic units, such as sulfonic and carboxyl groups, which are capable of attracting a greater number of silver ions, have shown good performance with respect to antibacterial activity [28,29]. Moreover, the presence of ionic groups on the polymer can mitigate the stabilization of Ag nanoparticles, decreasing the surface energy; once the nanoparticles in solution have been produced, the ionic polymeric units associate with the surface of the nanoparticles to establish a double layer of charge that stabilizes the particles themselves and prevents their aggregation. It is known that the complexing ability of silver ion with the amino group is stronger than that of the carboxyl group, and this should induce a greater stabilization of the obtained nanoparticles [30]. As in the case of bovine albumin, groups carrying sulfur, oxygen, and nitrogen mitigate the high surface energy of the nanoparticles during the reduction; moreover, the hydroxyl groups on cellulose help stabilize the particles. It is to be expected that the various hydrogels used in this work can behave this way and therefore, to varying degrees, can mitigate the stabilization of the silver nanoparticles obtained. 2. Results and Discussion 2.1. Protonation and Complex Formation Thermodynamics A preliminary potentiometric titration study for understanding the interaction strength of the different ionic groups present on the polymer was carried out mainly on the monomer precursors. The latter, being more soluble than the corresponding polymers, can give more information about the complexing ability towards silver ions in a wide pH range. As was to be expected, the N-acryloyl-L-phenylalanine (PHE) monomer exhibits no significant deviation of the titration curve in the presence and absence of silver ion (Figure1) in the low pH range involving the ionization of the carboxylic group. Figure 1. Potentiometric titration curves of monomer N-acryloyl-L-phenylalanine (PHE) in the absence (red filled) and in the presence (green filled) of Ag(I) ions. For comparison, the titration curves of nitric acid (brown open) and silver(I) ions (violet open) are also reported.
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